Semiologic subgroups of insulo-opercular seizures based on connectional architecture atlas.

OBJECTIVE: Insulo-opercular seizures are characterized by diverse semiology, related to the insula's multiple functional roles and extensive connectivity. We aimed to identify semiologic subgroups and correlate these with insulo-opercular subregions based on connectional architecture. METHODS: We retrospectively collected a large series of 37 patients with insulo-opercular seizures explored by stereoelectroencephalography (SEEG) from three epilepsy centers. A new human brain atlas (Brainnetome Atlas, BNA) based on both anatomic and functional connections was employed to segment insulo-opercular cortex. Semiology and SEEG changes were carefully reviewed and quantified. Principal component analysis and cluster analysis were used to correlate semiologic characteristics with insulo-opercular subregions. RESULTS: Four main semiologic subgroups were identified, organized along an anteroventral to posterodorsal axis based on BNA. Group 1 was characterized by epigastric sensation and/or integrated gestural motor behaviors with or without feelings of fear or rage, involving the anteroventral insular regions and mesial temporal lobes. Group 2 was characterized by auditory sensations and symmetric proximal/axial tonic signs involving the posteroventral temporal operculum. The characteristics of group 3 were orofacial and laryngeal signs, involving the intermediate insulo-opercular regions. The features of group 4 were somatosensory signs followed by nonintegrated gestural motor behaviors and/or asymmetric tonic signs involving the posterodorsal insulo-opercular regions with propagation to the mesial frontal lobes. Thus anteroventral seizure organizations predominantly showed limbic system semiology, whereas more posterodorsal regions were associated with semiology involving mainly the sensorimotor system. Subjective symptoms proved to be particularly discriminating factors. SIGNIFICANCE: Insulo-opercular seizures can be categorized in terms of clinical semiology and correlate with connectional architecture subregions along an anteroventral-posterodorsal axis in line with the cytoarchitectonic gradient rather than the gyral anatomy of the insula cortex. This provides new insights into facilitating differential diagnosis and presurgical localization but also highlights the importance of considering connectional architecture in determining neural correlates of complex semiologic patterns.

Rethinking cognition and behavior in the new classification for childhood epilepsy: Examples from frontal lobe and temporal lobe epilepsies.

The new approach to classification of the epilepsies emphasizes the role of dysfunction in networks in defining types of epilepsies. This paper reviews the structural and neuropsychological deficits in two types of childhood epilepsy: frontal lobe and temporal lobe epilepsy. The evidence for and against a pattern of specificity of deficits in executive function and memory associated with these two types of epilepsies is presented. The evidence varies with the methodologies used in the studies, but direct comparison of the two types of epilepsies does not suggest a clear-cut mapping of function onto structure. These findings are discussed in light of the concept of network dysfunction. The evidence supports the conceptualization of epilepsy as a network disease. Implications for future work in the neuropsychology of pediatric epilepsy are suggested. This article is part of a Special Issue entitled "The new approach to classification: Rethinking cognition and behavior in epilepsy".

Classification of EEG abnormalities in partial epilepsy with simultaneous EEG-fMRI recordings.

Scalp EEG recordings and the classification of interictal epileptiform discharges (IED) in patients with epilepsy provide valuable information about the epileptogenic network, particularly by defining the boundaries of the "irritative zone" (IZ), and hence are helpful during pre-surgical evaluation of patients with severe refractory epilepsies. The current detection and classification of epileptiform signals essentially rely on expert observers. This is a very time-consuming procedure, which also leads to inter-observer variability. Here, we propose a novel approach to automatically classify epileptic activity and show how this method provides critical and reliable information related to the IZ localization beyond the one provided by previous approaches. We applied Wave_clus, an automatic spike sorting algorithm, for the classification of IED visually identified from pre-surgical simultaneous Electroencephalogram-functional Magnetic Resonance Imagining (EEG-fMRI) recordings in 8 patients affected by refractory partial epilepsy candidate for surgery. For each patient, two fMRI analyses were performed: one based on the visual classification and one based on the algorithmic sorting. This novel approach successfully identified a total of 29 IED classes (compared to 26 for visual identification). The general concordance between methods was good, providing a full match of EEG patterns in 2 cases, additional EEG information in 2 other cases and, in general, covering EEG patterns of the same areas as expert classification in 7 of the 8 cases. Most notably, evaluation of the method with EEG-fMRI data analysis showed hemodynamic maps related to the majority of IED classes representing improved performance than the visual IED classification-based analysis (72% versus 50%). Furthermore, the IED-related BOLD changes revealed by using the algorithm were localized within the presumed IZ for a larger number of IED classes (9) in a greater number of patients than the expert classification (7 and 5, respectively). In contrast, in only one case presented the new algorithm resulted in fewer classes and activation areas. We propose that the use of automated spike sorting algorithms to classify IED provides an efficient tool for mapping IED-related fMRI changes and increases the EEG-fMRI clinical value for the pre-surgical assessment of patients with severe epilepsy.

The sleep manifestations of frontal lobe epilepsy.

Frontal lobe seizures have a tendency to occur from sleep, and in some cases occur exclusively (or almost exclusively) from sleep; these individuals are said to have nocturnal frontal lobe epilepsy (NFLE). NFLE can be difficult to distinguish clinically from various other sleep disorders, particularly parasomnias, which also present with paroxysmal motor activity in sleep. Here, the manifestations of frontal lobe epilepsy are reviewed in detail, with particular reference to the influence of sleep and the characteristics of NFLE. Key aspects of differential diagnosis are also considered, and the underlying mechanisms involved in NFLE discussed.

Quantitative and trajectory analysis of movement trajectories in supplementary motor area seizures of frontal lobe epilepsy.

The objectives of this study were to quantitatively analyze the movement trajectories of four types of supplementary motor area (SMA) seizures (hyperkinetic, tonic posturing, fencing posture, tonic head turning), and to compare the movement trajectories of SMA seizures with those of temporal lobe seizures and psychogenic nonepileptic seizures. Ten video/EEG recordings of each type of seizure were obtained. Imaging data collected by video/EEG monitoring were transformed into a digital matrix with image processing software and then transformed into a movement trajectory curve with MATLAB 6.5 software. From these movement trajectories, amplitude, frequency, proximal/distal limb amplitude ratios, and shoulder/abdominal amplitude ratios measurements were calculated. One-way ANOVA revealed statistically significant differences in average amplitude, as well as proximal/distal limb amplitude ratios, in SMA seizures when compared with those of temporal lobe seizures and psychogenic nonepileptic seizures. This study proved the feasibility of quantitative analysis of SMA seizures and suggests it should be further evaluated for its capability to distinguish different seizure semiologies for the diagnosis of epilepsy.

Whole-brain MRI phenotyping in dysplasia-related frontal lobe epilepsy.

OBJECTIVE: To perform whole-brain morphometry in patients with frontal lobe epilepsy and evaluate the utility of group-level patterns for individualized diagnosis and prognosis. METHODS: We compared MRI-based cortical thickness and folding complexity between 2 frontal lobe epilepsy cohorts with histologically verified focal cortical dysplasia (FCD) (13 type I; 28 type II) and 41 closely matched controls. Pattern learning algorithms evaluated the utility of group-level findings to predict histologic FCD subtype, the side of the seizure focus, and postsurgical seizure outcome in single individuals. RESULTS: Relative to controls, FCD type I displayed multilobar cortical thinning that was most marked in ipsilateral frontal cortices. Conversely, type II showed thickening in temporal and postcentral cortices. Cortical folding also diverged, with increased complexity in prefrontal cortices in type I and decreases in type II. Group-level findings successfully guided automated FCD subtype classification (type I: 100%; type II: 96%), seizure focus lateralization (type I: 92%; type II: 86%), and outcome prediction (type I: 92%; type II: 82%). CONCLUSION: FCD subtypes relate to diverse whole-brain structural phenotypes. While cortical thickening in type II may indicate delayed pruning, a thin cortex in type I likely results from combined effects of seizure excitotoxicity and the primary malformation. Group-level patterns have a high translational value in guiding individualized diagnostics.

Nocturnal paroxysmal arousals with motor behaviors during sleep: frontal lobe epilepsy or parasomnia?

Nocturnal paroxysmal arousals with motor behaviors have been described in a few individuals, and their possible epileptic origin as nocturnal frontal lobe seizures has been suggested. However, the clinical and polysomnographic differentiation from parasomnias and physiologic movements during sleep have not been clarified yet. In this study, we evaluated a group of patients with nocturnal motor behaviors and tried to characterize paroxysmal arousals. Thirty-four participants (mean [+/-SD] age 22.7 [+/-12.9] years) noting nocturnal motor agitation or behaviors and 12 healthy controls (mean age 24.1 [+/-3.1] years) underwent nocturnal polysomnography with video-tape recording and motor behaviors analysis. Arousals with motor attacks were classified as minimal, minor, or major depending on semiology, complexity, and duration of behaviors. All patients showed several minimal (e.g., scratching or rubbing the nose and the head) and minor (e.g., pelvic thrusting or swinging with dystonic component) attacks, and 53% also had major episodes (e.g., sudden elevation of the head and trunk from the bed with complex behaviors) occurring mainly in non-rapid eye movement sleep. In all the patients, motor attacks were characterized by stereotypy, sudden onset, short duration, and repetitiveness. In 80%, epileptiform abnormalities were found. All control subjects showed motor events, but they were fewer, slower, nonstereotyped, and semiologically different from the patients'. No significant difference in conventional sleep parameters between the two groups were found. Paroxysmal arousals with motor behaviors probably represent a particular form of nocturnal frontal lobe epilepsy rather than an unusual parasomnia. The semiologic characteristics of these type of arousals are difficult to recognize and differentiate from physiologic movements or parasomnias without video-polygraphic analysis.

Structural lesions of the frontal lobe. Manifestations, classification, and prognosis.

Newer imaging methods, particularly MRI, are recognizing increasing numbers of frontal static and progressive lesions in patients in whom recurrent seizures are the presenting and only symptoms. Surgical results in terms of controlling frontal seizures are improving and becoming comparable to those achieved in the temporal lobe. The results following removal of discrete frontal lesions are superior to those with more diffuse lesions or without demonstrable lesions. Stereotaxic surgery and microsurgical techniques are allowing safer excisions from formerly inaccessible areas or adjacent to areas of essential function. These advances have increased the number of candidates who benefit from successful frontal lobe surgery. The types of clinical seizures in patients with discrete local frontal lesions usually conform with five of the seven anatomically named seizure types described in the 1989 International Classification of Epilepsies and Epileptic Syndromes (supplemental motor seizures, anterior frontopolar region, dorsolateral, and motor cortex). Too few cases with discrete lesions were found with sufficiently detailed seizure descriptions of possible orbitofrontal and cingulate origin to allow separate categorizations. In those cases symptoms and signs, such as autonomic, mood and affect, gestural automatisms, and versive movements preceding the automatisms, did not seem to differentiate orbitofrontal and anterior cingulate lesion cases from each other or from those in other areas of the anterior third of the frontal lobe.

Frontal lobe epilepsy: the next frontier.

Frontal lobe epilepsy, the great new epileptological challenge, presents enormous difficulties that still preclude a more profound understanding at the present time. The major subdivision of the frontal lobe into a prefrontal and premotor portion is the first step toward a better and yet limited comprehension of the frontal lobe epilepsies. Prefrontal implies higher mental functions (e.g., ictal forced thinking); rapid generalization to full grand mal evolves quite often from prefrontal foci. The frontal accentuation of classical generalized 3/sec spike-wave absences adds to the conceptual difficulties of the frontal lobe epilepsies. The unique type of disturbed consciousness in classical absences is presumed to be based upon ictal "suspension of the working memory." Limbic components (via orbitofrontal and cingulate mechanisms) also play an important role. Correlations between ictal semiologies and regional frontal lobe functions are still quite controversial.

Use of statistical parametric mapping of (18) F-FDG-PET in frontal lobe epilepsy.

AIM: Evaluation of the use of statistical parametrical mapping (SPM) of FDG-PET for seizure lateralization in frontal lobe epilepsy. PATIENTS: 38 patients with suspected frontal lobe epilepsy supported by clinical findings and video-EEG monitoring. METHOD: Statistical parametrical maps were generated by subtraction of individual scans from a control group, formed by 16 patients with negative neurological/psychiatric history and no abnormalities in the MR scan. The scans were also analyzed visually as well as semiquantitatively by manually drawn ROIs. RESULTS: SPM showed a better accordance to the results of surface EEG monitoring compared with visual scan analysis and ROI quantification. In comparison with intracranial EEG recordings, the best performance was achieved by combining the ROI based quantification with SPM analysis. CONCLUSION: These findings suggest that SPM analysis of FDG-PET data could be a useful as complementary tool in the evaluation of seizure focus lateralization in patients with supposed frontal lobe epilepsy.

Cingulate epilepsy: report of 3 electroclinical subtypes with surgical outcomes.

IMPORTANCE: The literature on cingulate gyrus epilepsy in the magnetic resonance imaging era is limited to case reports and small case series. To our knowledge, this is the largest study of surgically confirmed epilepsy arising from the anterior or posterior cingulate region. OBJECTIVE: To characterize the clinical and electrophysiological findings of epilepsies arising from the anterior and posterior cingulate gyrus. DESIGN, SETTING, AND PARTICIPANTS: We studied consecutive cingulate gyrus epilepsy cases identified retrospectively from the Cleveland Clinic and University of Texas Southwestern Medical Center epilepsy databases from 1992 to 2009. Participants included 14 consecutive cases of cingulate gyrus epilepsies confirmed by restricted magnetic resonance image lesions and seizure freedom or marked improvement following lesionectomy. MAIN OUTCOMES AND MEASURES: The main outcome measure was improvement in seizure frequency following surgery. The clinical, video electroencephalography, neuroimaging, pathology, and surgical outcome data were reviewed. RESULTS: All 14 patients had cingulate epilepsy confirmed by restricted magnetic resonance image lesions and seizure freedom or marked improvement following lesionectomy. They were divided into 3 groups based on anatomical location of the lesion and corresponding seizure semiology. In the posterior cingulate group, all 4 patients had electroclinical findings suggestive of temporal origin of the epilepsy. The anterior cingulate cases were divided into a typical (Bancaud) group (6 cases with hypermotor seizures and infrequent generalization with the presence of fear, laughter, or severe interictal personality changes) and an atypical group (4 cases presenting with simple motor seizures and a tendency for more frequent generalization and less-favorable long-term surgical outcome). All atypical cases were associated with an underlying infiltrative astrocytoma. CONCLUSIONS AND RELEVANCE: Posterior cingulate gyrus epilepsy may present with electroclinical findings that are suggestive of temporal lobe epilepsy and can be considered as another example of pseudotemporal epilepsies. The electroclinical presentation and surgical outcome of lesional anterior cingulate epilepsy is possibly influenced by the underlying pathology. This study highlights the difficulty in localizing seizures arising from the cingulate gyrus in the absence of a magnetic resonance image lesion.

Subclinical abnormal gyration pattern, a potential anatomic marker of epileptogenic zone in patients with magnetic resonance imaging-negative frontal lobe epilepsy.

BACKGROUND: Epilepsy surgery for magnetic resonance imaging (MRI)-negative patients has a less favorable outcome. OBJECTIVE: Detection of subclinical abnormal gyration (SAG) patterns and their potential contribution to assessment of the topography of the epileptogenic zone (EZ) is addressed in MRI-negative patients with frontal lobe epilepsy. METHODS: Between September 1998 and July 2005, 12 MRI-negative frontal lobe epilepsy patients underwent stereoelectroencephalography with postcorticectomy follow-up of longer than 1 year (average, 3.3 years). Original software (BrainVISA/Anatomist, http://brainvisa.info) trained on a database of normal volunteers was used to determine which sulci had morphology out of the normal range (SAG). Topography of the EZ, SAG pattern, corticectomy, postoperative seizure control, and histopathology were analyzed. RESULTS: At last follow-up, 8 of 12 patients (66.7%) were Engel class I (7 IA and 1 IB), 2 class II, and 2 class IV. Small focal cortical dysplasia was histologically diagnosed in 9 of the 12 patients (75%), including 7 of 8 seizure-free patients (87.5%). A SAG pattern was found to be in the EZ area in 9 patients (75%), in the ipsilateral frontal lobe out of the EZ in 2, and limited to the contralateral hemisphere in 1. CONCLUSION: SAG patterns appear to be associated with the topography of the EZ in MRI-negative frontal lobe epilepsy and may have a useful role in preoperative assessment. Small focal cortical dysplasia not detected with MRI is often found on histopathological examination, particularly in the depth of the posterior part of the superior frontal sulcus and intermediate frontal sulcus, suggesting a specific developmental critical zone in these locations.

Interobserver reliability of video recording in the diagnosis of nocturnal frontal lobe seizures.

BACKGROUND: Nocturnal frontal lobe seizures (NFLS) show one or all of the following semeiological patterns: (1) paroxysmal arousals (PA: brief and sudden recurrent motor paroxysmal behavior); (2) hyperkinetic seizures (HS: motor attacks with complex dyskinetic features); (3) asymmetric bilateral tonic seizures (ATS: motor attacks with dystonic features); (4) epileptic nocturnal wanderings (ENW: stereotyped, prolonged ambulatory behavior). OBJECTIVE: To estimate the interobserver reliability (IR) of video-recording diagnosis in patients with suspected NFLS among sleep medicine experts, epileptologists, and trainees in sleep medicine. METHODS: Sixty-six patients with suspected NFLS were included. All underwent nocturnal video-polysomnographic recording. Six doctors (three experts and three trainees) independently classified each case as "NFLS ascertained" (according to the above specified subtypes: PA, HS, ATS, ENW) or "NFLS excluded". IR was calculated by means of Kappa statistics, and interpreted according to the standard classification (0.0-0.20 = slight agreement; 0.21-0.40 = fair; 0.41-0.60 = moderate; 0.61-0.80 = substantial; 0.81-1.00 = almost perfect). RESULTS: The observed raw agreement ranged from 63% to 79% between each pair of raters; the IR ranged from "moderate" (kappa = 0.50) to "substantial" (kappa = 0.72). A major source of variance was the disagreement in distinguishing between PA and nonepileptic arousals, without differences in the level of agreement between experts and trainees. CONCLUSIONS: Among sleep experts and trainees, IR of diagnosis of NFLS, based on videotaped observation of sleep phenomena, is not satisfactory. Explicit video-polysomnographic criteria for the classification of paroxysmal sleep motor phenomena are needed.